Cap 15

1, the so-called 
 peristomial polykinety , and the proter’s paroral 
or haplokinety . A new germinal kinety prolifer-
ates from the paroral of both filial cells prior to 
completion of stomatogenesis. This pattern has 
been confirmed for Astylozoon (Guinea, Sola, 
Rueda, & Fernández-Galiano, 1988), Carchesium
(Esteban & Fernández-Galiano, 1989), Opercularia
(Fernández-Galiano, Esteban, & Munoz, 1988), 
Opisthonecta (Sola, Guinea, & Fernández-Galiano, 
1985), and Thuricola (Eperon, 1980). Foissner 
(1996b) characterizes this as an ophryobuccokinetal 
stomatogenesis since the opisthe’s oral apparatus 
derives from an ophryo − or germinal kinety , sug-
gesting homologies to the process in peniculines , 
but also to that of the scuticociliates . Indeed, it is to 
the latter group, and particularly the thigmotrichs , 
to which the common ancestry of the peritrichs 
has been linked (Fauré-Fremiet, 1950a; Lom, 
1964). We currently need some gene sequences 
from thigmotrichs to explicitly test this hypothesis. 
However, the gene sequence database currently 
does not support it: peritrichs are consistently a 
strongly supported sister clade to the hymenos-
tomes and not to the scuticociliates (Affa’a et al., 
2004; Miao et al., 2004b). 
 The last two groups of oligohymenophore-
ans , the apostomes and astomes , are problematic 
because they are so divergent. Astomes , of course, 
have no stomatogenesis, since by definition they 
have no mouth. They divide transversely, equally or 
unequally (Fig. 15.5). In the latter case, they may 
remain attached as chains of cells or catenoid “col-
onies” (Beers, 1938; de Puytorac, 1954, 1994g). 
Subsequent cell growth and division may involve 
only the anterior cell (e.g., Hoplitophrya ) or each 
filial cell may grow and divide (e.g., Cepedietta ) 
but not separate (de Puytorac, 1994g). 
 Apostome division morphogenesis demonstrates 
no clear homologies with other oligohymenopho-
reans , presumably a result of the highly unusual 
life cycle of these ciliates. “Stomatogenesis” and 
morphogenesis during the life cycle have been 
studied in Hyalophysa using protargol staining 
(Fig. 15.11) (Bradbury, Song, & Zhang, 1997; 
Landers, 1986). The anterior kinety, kinety a , 
plays a central role in the replication of cortical 
structures. It elongates by replication of a small, 
anterior fragment in the trophont , and apparently 
differentiates into three bipolar kineties, named a , 
b , and c . The latter kinety dedifferentiates com-
pletely, b may differentiate as the paroral , and a
provides continuity as the kinety a for the next 
round of fission (Bradbury et al., 1997). Bradbury 
et al. (1997) noted that kinety a in Foettingeria
derives from Kinety 1. Thus, this is a kind 
of monoparakinetal stomatogenesis , like that 
of Tetrahymena , since kinety a provides an 
oral structure, the paroral homologue . This is 
also consistent with preliminary gene sequence 
data that place apostomes within the oligohy-
menophorean clade, although not close to the 
 hymenostomes (J.C. Clamp et al., 2008; Lynn 
et al., 2005). 
 A discussion of division morphogenesis of oli-
gohymenophoreans would not be complete without 
some reference to the extensive literature on the 
cell and developmental biology of the process, 
most recently reviewed by Frankel (1989, 1991). 
Simply, the process can be viewed as a duplication 
15.5 Division and Morphogenesis 319
320 15. Subphylum 2. INTRAMACRONUCLEATA: Class 9. OLIGOHYMENOPHOREA
of structure controlled at two major levels – at the 
level of the organelles and organellar complexes 
and at the level of the cell as a whole. At the 
 organellar complex level , the working hypoth-
esis has long been that the local environment 
and pre-existing structure play determining roles, 
so-called structural guidance or cytotaxis (Frankel, 
1989; Sonneborn, 1964; Williams, 1986). There is 
now convincing evidence for this in the propaga-
tion, over many cell cycles, of a patch of inverted 
somatic kineties (Beisson & Sonneborn, 1965; Ng 
& Williams, 1977). Furthermore, successful repli-
cation is dependent upon the presence of specific, 
kinetosome-associated structures (Iftode & Fleury-
Aubusson, 2003; Kaczanowska et al., 1996). The 
inversion of these kinetids also causes the beat cycle 
of their cilia to be opposite to those of adjacent, 
normally-oriented kinetids (Tamm, Sonneborn, & 
Dippell, 1975). For the Paramecium cell as a whole, 
there is suggestive evidence that morphogenetic 
waves , originating from the oral apparatus and fis-
sion furrow, induce duplication and reorganization 
processes (Iftode et al., 1989). Migration of the 
new oral structures, essential to the completion of 
normal division in all oligohymenophoreans but 
 hymenostomes , depends upon proper disassembly 
and reassembly of cortical structures (Kaczanowska 
et al., 1995). When the oral development in the two 
cells is almost complete, cytokinesis occurs, accom-
panied by the appearance of a contractile ring of 
microfilaments at the fission furrow (Eperon, 1985; 
Jerka-Dziadosz, 1981c; Yasuda, Numata, Ohnishi, 
& Watanabe, 1980). Assembly of a functional 
 contractile ring depends upon Ca 2+ and several 
proteins, including calmodulin and actin (Gonda & 
Numata, 2002; Williams et al., 2006). 
 Oligohymenophoreans have limited powers of 
regeneration. Nevertheless, as in other classes, 
regeneration after microsurgery has been demon-
strated in some peniculines (Chen-Shan, 1979) and 
 hymenostomes (Mugard & Lorsignol, 1956). 
 15.6 Nuclei, Sexuality and Life 
Cycle
 The oligohymenophoreans present a broad diver-
sity of forms in the macronucleus . Typically, the 
 macronucleus is single and globular to ellipsoid 
(Figs. 15.2–15.5). Variations do exist: peritrichs 
are typified by the horseshoe- or band-shaped 
 macronucleus (Fig. 15.3) (Lom, 1994); astomes 
may have a macronucleus extending along the 
entire length of the body, sometimes with irregu-
lar extensions (Fig. 15.5) (de Putyorac, 1994g); a 
rare scuticociliate can have multiple fragments of 
the macronucleus (Lynn & Frombach, 1987); and 
 apostomes demonstrate a variety of macronuclear 
forms with one form showing a complex network 
(Fig. 15.2) (de Puytorac, 1994h). 
 The micronucleus is typically solitary, although 
some species are typified by having two micronu-
clei. In rare exceptions, over 40 micronuclei have 
been observed in particularly large-bodied forms 
(Lynch, 1929; Lynn & Berger, 1973). The micro-
nucleus of oligohymenophoreans can have from 
five chromosomes in Tetrahymena (Ray, 1956) 
to several hundreds in Paramecium species, and 
some Paramecium species may be polyploid (Aury 
et al., 2006; Raikov, 1982). Micronuclear morphol-
ogy can vary both between and within genera. 
For example, four different types of micronuclei 
have been identified by Fokin (1997) among ten 
different Paramecium species: these are vesicular, 
endosomal, chromosomal, and compact types. 
 Macronuclear ploidy varies typically with the sizes 
of the cell and the macronucleus: the larger mac-
rostome species of Tetrahymena may be 450 × n; 
larger Paramecium species over 850 × n; and the 
large trophonts of Ichthyophthirius set an oligohy-
menophorean record of 6,300 × n (Raikov). 
 Both kinds of nuclei in oligohymenophoreans 
divide with the aid of microtubules. Intramacro-
nuclear microtubules have been observed in dividing
Paramecium and Tetrahymena (Nilsson, 1976; 
Tucker, Beisson, Roche, & Cohen, 1980) and 
 myosin has been implicated by immunofluorescence 
studies (Hauser, Beinbrech, Gröschel-Stewart, & 
Jockusch, 1975). Analysis of mutant phenotypes 
of Paramecium and drug and heat treatments of 
Tetrahymena provided support for the model that 
microtubular sliding elongates the macronucleus 
(Cohen, Beisson, & Tucker, 1980; Nilsson, 1976). 
Nevertheless,